Abstract
Aims
Invasive plants not only alter aboveground biodiversity but also belowground microbial community composition to facilitate their growth and competitiveness. However, how plant invasion affects soil microbial resource limitation and metabolic activity, and their linkages with litter and soil stoichiometries remain largely unknown.
Methods
We investigated the carbon (C): nitrogen (N): phosphorus (P) stoichiometries of litter, soil, microbe and extracellular enzymes, composition of main microbial groups and substrate utilization rate in a subtropical forest invaded by Moso bamboo (Phyllostachys edulis) and those in adjacent broadleaf and mixed bamboo-broadleaf forests.
Results
Bamboo invasion significantly decreased annual litter production, litter C: P and N: P ratios, and soil C:N and C:P ratios, whereas increased microbial biomass C:N and C:P ratios, resulting in decreased C:N and C:P imbalances between soil microorganisms and their resources. Bamboo invasion decreased the N and P acquiring enzymes activities, mitigated the status of microbial N and P limitation as indicated by enzymatic stoichiometry, and caused a higher C use efficiency. Soil microbial community structure was shifted towards a lower fungi: bacteria (F:B) ratio in bamboo forest. Bamboo forest soil showed a lower capacity of microbes to use N-rich resources in comparison to C-rich resources. Structural equation modeling suggested a direct and negative effect of C:N imbalance on microbial N limitation and metabolic capacity.
Conclusions
This study suggests the importance of stoichiometric imbalance between decomposers and their resources in regulating soil microbial community structure and enzyme activities following plant invasion.
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References
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46
Bai S, Zhou G, Wang Y, Liang Q, Chen J, Cheng Y, Shen R (2013) Plant species diversity and dynamics in forests invaded by moso bamboo (Phyllostachys edulis) in Tianmu Mountain nature reserve. Biodivers Sci 21:288–295 (In Chinese)
Bardgett RD, van der Putten WH (2014) Belowground biodiversity and ecosystem functioning. Nature 515:505–511
Bossio D, Scow K (1998) Impacts of carbon and flooding on soil microbial communities: phospholipid fatty acid profiles and substrate utilization patterns. Microb Ecol 35:265–278
Campbell CD, Chapman SJ, Cameron CM, Davidson MS, Potts JM (2003) A rapid microtiter plate method to measure carbon dioxide evolved from carbon substrate amendments so as to determine the physiological profiles of soil microbial communities by using whole soil. Appl Environ Microb 69:3593–3599
Chang EH, Chiu CY (2015) Changes in soil microbial community structure and activity in a cedar plantation invaded by moso bamboo. Appl Soil Ecol 91:1–7
Chen J, Sun X, Li L, Liu X, Zhang B, Zheng J, Pan G (2016) Change in active microbial community structure, abundance and carbon cycling in an acid rice paddy soil with the addition of biochar. Eur J Soil Sci 67:857–867
Chen J, Li S, Liang C, Xu Q, Li Y, Qin H, Fuhrmann JJ (2017) Response of microbial community structure and function to short-term biochar amendment in an intensively managed bamboo (Phyllostachys praecox) plantation soil: effect of particle size and addition rate. Sci Total Environ 574:24–33
Chen H, Li D, Xiao K, Wang K (2018a) Soil microbial processes and resource limitation in karst and non-karst forests. Funct Ecol 32:1400–1409
Chen L, Liu L, Mao C, Qin S, Wang J, Liu F, Blagodatsky S, Yang G, Zhang Q, Zhang D, Yu J, Yang Y (2018b) Nitrogen availability regulates topsoil carbon dynamics after permafrost thaw by altering microbial metabolic efficiency. Nat Commun 9:3951
Chen J, Chen D, Xu Q, Fuhrmann JJ, Li L, Pan G, Li Y, Qin H, Liang C, Sun X (2019) Organic carbon quality, composition of main microbial groups, enzyme activities, and temperature sensitivity of soil respiration of an acid paddy soil treated with biochar. Biol Fertil Soils 55:185–197
Clemmensen KE, Bahr A, Ovaskainen O, Dahlberg A, Ekblad A, Wallander H, Stenlid J, Finlay RD, Wardle DA, Lindahl BD (2013) Roots and associated fungi drive long-term carbon sequestration in boreal forest. Science 339:1615–1618
Cleveland CC, Liptzin D (2007) C:N:P stoichiometry in soil: is there a "Redfield ratio" for the microbial biomass? Biogeochemistry 85:235–252
Dawson W, Schrama M (2016) Identifying the role of soil microbes in plant invasions. J Ecol 104:1211–1218
Dong H, Ge J, Sun K, Wang B, Xue J, Wakelin SA, Wu J, Sheng W, Liang C, Xu Q, Jiang P, Chen J, Qin H (2021) Change in root-associated fungal communities affects soil enzymatic activities during Pinus massoniana forest development in subtropical China. Forest Ecol Manag 482:118817
Ehrenfeld JG (2010) Ecosystem consequences of biological invasions. Annu Rev Ecol Syst 41:59–80
Ekblad A, Nordgren A (2002) Is growth of soil microorganisms in boreal forests limited by carbon or nitrogen availability? Plant Soil 242:115–122
Elser JJ, Bracken MES, Cleland EE, Gruner DS, Harpole WS, Hillebrand H, Ngai JT, Seabloom EW, Shurin JB, Smith JE (2007) Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine, and terrestrial ecosystems. Ecol Lett 10:1135–1142
Fanin N, Fromin N, Buatois B, Hattenschwiler S (2013) An experimental test of the hypothesis of non-homeostatic consumer stoichiometry in a plant litter-microbe system. Ecol Lett 16:764–772
Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1364
Frost PC, Benstead JP, Cross WF, Hillebrand H, Larson JH, Xenopoulos MA, Yoshida T (2006) Threshold elemental ratios of carbon and phosphorus in aquatic consumers. Ecol Lett 9:774–779
Frostegård A, Bååth E (1996) The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biol Fertil Soils 22:59–65
Guo K, Zhao Y, Liu Y, Chen J, Wu Q, Ruan Y, Li S, Shi J, Zhao L, Sun X, Liang C, Xu Q, Qin H (2020) Pyrolysis temperature of biochar affects ecoenzymatic stoichiometry and microbial nutrient-use efficiency in a bamboo forest soil. Geoderma 363:114162
Hooper D, Coughlan J, Mullen M (2008) Structural equation modelling: guidelines for determining model fit. Electr J Business Res Methods 6:53–60
Koranda M, Kaiser C, Fuchslueger L, Kitzler B, Sessitsch A, Zechmeister-Boltenstern S, Richter A (2014) Fungal and bacterial utilization of organic substrates depends on substrate complexity and N availability. FEMS Microbiol Ecol 87:142–152
Lekberg Y, Gibbons SM, Rosendahl S, Ramsey PW (2013) Severe plant invasions can increase mycorrhizal fungal abundance and diversity. ISME J 7:1424–1433
Li Y, Li Y, Chang SX, Xu Q, Guo Z, Gao Q, Qin Z, Yang Y, Chen J, Liang X (2017) Bamboo invasion of broadleaf forests altered soil fungal community closely linked to changes in soil organic C chemical composition and mineral N production. Plant Soil 418:507–521
Liu X, Siemann E, Cui C, Liu Y, Guo X, Zhang L (2019) Moso bamboo (Phyllostachys edulis) invasion effects on litter, soil and microbial PLFA characteristics depend on sites and invaded forests. Plant Soil 438:85–99
Lu RK (2000) Methods of soil and agro-chemical analysis. China Agricultural Science and Technology Press, Beijing (in Chinese)
Manzoni S, Jackson RB, Trofymow JA, Porporato A (2008) The global stoichiometry of litter nitrogen mineralization. Science 321:684–686
Manzoni S, Trofymow JA, Jackson RB, Porporato A (2010) Stoichiometric controls on carbon, nitrogen, and phosphorus dynamics in decomposing litter. Ecol Monogr 80:89–106
Manzoni S, Taylor P, Richter A, Porporato A, Agren GI (2012) Environmental and stoichiometric controls on microbial carbon-use efficiency in soils. New Phytol 196:79–91
Moorhead DL, Rinkes ZL, Sinsabaugh RL, Weintraub MN (2013) Dynamic relationships between microbial biomass, respiration, inorganic nutrients and enzyme activities: informing enzyme-based decomposition models. Front Microbiol 4:223
Mooshammer M, Wanek W, Haemmerle I, Fuchslueger L, Hofhansl F, Knoltsch A, Schnecker J, Takriti M, Watzka M, Wild B, Keiblinger KM, Zechmeister-Boltenstern S, Richter A (2014a) Adjustment of microbial nitrogen use efficiency to carbon: nitrogen imbalances regulates soil nitrogen cycling. Nat Commun 5:3694
Mooshammer M, Wanek W, Zechmeister-Boltenstern S, Richter A (2014b) Stoichiometric imbalances between terrestrial decomposer communities and their resources: mechanisms and implications of microbial adaptations to their resources. Front Microbiol 5:22
Niu Y, Chai R, Jin G, Wang H, Tang C, Zhang Y (2013) Responses of root architecture development to low phosphorus availability: a review. Ann Bot -London 112:391–408
Olsen SR, Sommers LE (1982) Phosphorus. In: Page AL, Miller RH, Keeney DR (eds), Methods of Soil Analysis. Part 2. Chemical and Microbiological Properties. Agronomy, No. 9. American Society of Agronomy and Soil Science Society of America, Madison, pp. 403-430
Qin H, Niu L, Wu Q, Chen J, Li Y, Liang C, Xu Q, Fuhrmann JJ, Shen Y (2017) Bamboo forest expansion increases soil organic carbon through its effect on soil arbuscular mycorrhizal fungal community and abundance. Plant Soil 420:407–421
Reinhart KO, Callaway RM (2006) Soil biota and invasive plants. New Phytol 170:445–457
Ricciardi A, Blackburn TM, Carlton JT, Dick JTA, Hulme PE, Iacarella JC et al (2017) Invasion science: a horizon scan of emerging challenges and opportunities. Trends Ecol Evol 32:464–474
Riggs CE, Hobbie SE (2016) Mechanisms driving the soil organic matter decomposition response to nitrogen enrichment in grassland soils. Soil Biol Biochem 99:54–65
Rodgers VL, Wolfe BE, Werden LK, Finzi AC (2008) The invasive species Alliaria petiolata (garlic mustard) increases soil nutrient availability in northern hardwood-conifer forests. Oecologia 157:459–471
Saiya-Cork KR, Sinsabaugh RL, Zak DR (2002) The effects of long term nitrogen deposition on extracellular enzyme activity in an Acer saccharum forest soil. Soil Biol Biochem 34:1309–1315
Schaeffer SM, Ziegler SE, Belnap J, Evans RD (2012) Effects of Bromus tectorum invasion on microbial carbon and nitrogen cycling in two adjacent undisturbed arid grassland communities. Biogeochemistry 111:427–441
Sinsabaugh RL, Lauber CL, Weintraub MN, Ahmed B, Allison SD, Crenshaw C, Contosta AR, Cusack D, Frey S, Gallo ME, Gartner TB, Hobbie SE, Holland K, Keeler BL, Powers JS, Stursova M, Takacs-Vesbach C, Waldrop MP, Wallenstein MD, Zak DR, Zeglin LH (2008) Stoichiometry of soil enzyme activity at global scale. Ecol Lett 11:1252–1264
Sinsabaugh RL, Hill BH, Follstad Shah JJ (2009) Ecoenzymatic stoichiometry of microbial organic nutrient acquisition in soil and sediment. Nature 462:795
Sinsabaugh RL, Manzoni S, Moorhead DL, Richter A (2013) Carbon use efficiency of microbial communities: stoichiometry, methodology and modelling. Ecol Lett 16:930–939
Sinsabaugh RL, Turner BL, Talbot JM, Waring BG, Powers JS, Kuske CR, Moorhead DL, Shah JJF (2016) Stoichiometry of microbial carbon use efficiency in soils. Ecol Monogr 86:172–189
Sistla SA, Schimel JP (2012) Stoichiometric flexibility as a regulator of carbon and nutrient cycling in terrestrial ecosystems under change. New Phytol 196:68–78
Six J, Frey SD, Thiet RK, Batten KM (2006) Bacterial and fungal contributions to carbon sequestration in agroecosystems. Soil Sci Soc Am J 70:555–569
Song Q, Ouyang M, Yang Q, Lu H, Yang G, Chen F, Shi JM (2016) Degradation of litter quality and decline of soil nitrogen mineralization after moso bamboo (Phyllostachys pubscens) expansion to neighboring broadleaved forest in subtropical China. Plant Soil 404:113–124
Spohn M, Chodak M (2015) Microbial respiration per unit biomass increases with carbon-to-nutrient ratios in forest soils. Soil Biol Biochem 81:128–133
Stark S, Männistö MK, Eskelinen A (2014) Nutrient availability and pH jointly constrain microbial extracellular enzyme activities in nutrient-poor tundra soils. Plant Soil 383:373–385
Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, Princeton
Struecker J, Joergensen RG (2015) Microorganisms and their substrate utilization patterns in topsoil and subsoil layers of two silt loams, differing in soil organic C accumulation due to colluvial processes. Soil Biol Biochem 91:310–317
Touyama Y, Yamamoto T, Nakagoshi N (1998) Myrmecofaunal change with bamboo invasion into broadleaf forests. J Forest Res 3:155–159
van der Bom F, Nunes I, Raymond NS, Hansen V, Bonnichsen L, Magid J, Nybroe O, Jensen LS (2018) Long-term fertilisation form, level and duration affect the diversity, structure and functioning of soil microbial communities in the field. Soil Biol Biochem 122:91–103
Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass-C. Soil Biol Biochem 19:703–707
Vilà M, Espinar JL, Hejda M, Hulme PE, Jarošík V, Maron JL, Pergl J, Schaffner U, Sun Y, Pyšek P (2011) Ecological impacts of invasive alien plants: a meta-analysis of their effects on species, communities and ecosystems. Ecol Lett 14:702
Wang X, Sasaki A, Toda M, Nakatsubo T (2016) Changes in soil microbial community and activity in warm temperate forests invaded by moso bamboo (Phyllostachys pubescens). J For Res 21:235–243
Waring BG, Weintraub SR, Sinsabaugh RL (2014) Ecoenzymatic stoichiometry of microbial nutrient acquisition in tropical soils. Biogeochemistry 117:101–113
Wei X, Zhu Z, Liu Y, Luo Y, Deng Y, Xu X, Liu S, Richter A, Shibistova O, Guggenberger G, Wu J, Ge T (2020) C:N:P stoichiometry regulates soil organic carbon mineralization and concomitant shifts in microbial community composition in paddy soil. Biol Fertil Soils 56:1093–1107
Wild B, Schnecker J, Knoltsch A, Takriti M, Mooshammer M, Gentsch N, Mikutta R, Alves RJE, Gittel A, Lashchinskiy N, Richter A (2015) Microbial nitrogen dynamics in organic and mineral soil horizons along a latitudinal transect in western Siberia. Global Biogeochem Cy 29:567–582
World Reference Base for Soil Resources (WRB) (2006) A framework for international classification, correlation and communication. Food and Agriculture Organization of the United Nations, Rome
Xu QF, Jiang PK, Wu JS, Zhou GM, Shen RF, Fuhrmann J (2015) Bamboo invasion of native broadleaf forest modified soil microbial communities and diversity. Biol Invasions 17:433–444
Xu QF, Liang CF, Chen JH, Li YC, Qin H, Fuhrmann JJ (2020) Rapid bamboo invasion (expansion) and its effects on biodiversity and soil processes. Global Ecol Conserv 21:e00787
Yuan X, Niu D, Gherardi LA, Liu Y, Wang Y, Elser JJ, Fu H (2019) Linkages of stoichiometric imbalances to soil microbial respiration with increasing nitrogen addition: evidence from a long-term grassland experiment. Soil Biol Biochem 138:107580
Zak DR, Pregitzer KS, Curtis PS, Holmes WE (2000) Atmospheric CO2 and the composition and function of soil microbial communities. Ecol Appl 10:47–59
Zechmeister-Boltenstern S, Keiblinger KM, Mooshammer M, Peñuelas J, Richter A, Sardans J, Wanek W (2015) The application of ecological stoichiometry to plant–microbial–soil organic matter transformations. Ecol Monogr 85:133–155
Zelles L (1997) Phospholipid fatty acid profiles in selected members of soil microbial communities. Chemosphere 35:275–294
Zhang P, Li B, Wu J, Hu S (2019) Invasive plants differentially affect soil biota through litter and rhizosphere pathways: a meta-analysis. Ecol Lett 22:200–210
Zhu Z, Ge T, Liu S, Hu Y, Ye R, Xiao M, Tong C, Kuzyakov Y, Wu J (2018a) Rice rhizodeposits affect organic matter priming in paddy soil: the role of N fertilization and plant growth for enzyme activities, CO2 and CH4 emissions. Soil Biol Biochem 116:369–377
Zhu Z, Ge T, Luo Y, Liu S, Xu X, Tong C, Shibistova O, Guggenberger G, Wu J (2018b) Microbial stoichiometric flexibility regulates rice straw mineralization and its priming effect in paddy soil. Soil Biol Biochem 121:67–76
Acknowledgements
We thank the anonymous reviewers for their very valuable comments in improving both the language and scientific quality of the manuscript. This work was funded by the National Natural Science Foundation of China (41977083, 31971631), the Fundamental Research Funds for the Provincial Universities of Zhejiang (2020YQ004), the Natural Science Foundation of Zhejiang Province (LY20C160003).
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Highlights
1. Bamboo invasion changed litter and soil stoichiometries in a broadleaf forest.
2. Bamboo invasion mitigated microbial N and P limitation and increased CUE.
3. Bamboo invasion changed composition of main microbial groups and activity.
4. Mitigated N and P limitation was closely linked with litter and soil quality.
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Zhao, Y., Liang, C., Shao, S. et al. Linkages of litter and soil C:N:P stoichiometry with soil microbial resource limitation and community structure in a subtropical broadleaf forest invaded by Moso bamboo. Plant Soil 465, 473–490 (2021). https://doi.org/10.1007/s11104-021-05028-2
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DOI: https://doi.org/10.1007/s11104-021-05028-2